Higher-Order Assembly of Microtubules by Counterions: From Hexagonal Bundles to Living Necklaces

Cellular factors tightly regulate the architecture of bundles of filamentous cytoskeletal proteins, giving rise to assemblies with distinct morphologies and physical properties, and a similar control of the supramolecular organization of nanotubes and nanorods in synthetic materials is highly desira...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 101; no. 46; pp. 16099 - 16103
Main Authors Needleman, Daniel J., Ojeda-Lopez, Miguel A., Raviv, Uri, Miller, Herbert P., Wilson, Leslie, Safinya, Cyrus R., Chandler, David
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 16.11.2004
National Acad Sciences
SeriesFrom the Cover
Subjects
Animals
Biophysical Phenomena
Biophysics
Cations
Cattle
Dimers
Divalent cations
In Vitro Techniques
Ions
Macromolecular Substances
Materials
Microscopy, Electron
Microtubule-Associated Proteins - chemistry
Microtubule-Associated Proteins - metabolism
Microtubules
Microtubules - chemistry
Microtubules - metabolism
Microtubules - ultrastructure
Models, Biological
Nanostructures
Nanotubes
Necklaces
Physical Sciences
Scattering, Radiation
Static Electricity
Synchrotrons
Topology
Tubulin - chemistry
Tubulin - metabolism
X-Ray Diffraction
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Summary:Cellular factors tightly regulate the architecture of bundles of filamentous cytoskeletal proteins, giving rise to assemblies with distinct morphologies and physical properties, and a similar control of the supramolecular organization of nanotubes and nanorods in synthetic materials is highly desirable. However, it is unknown what principles determine how macromolecular interactions lead to assemblies with defined morphologies. In particular, electrostatic interactions between highly charged polyelectrolytes, which are ubiquitous in biological and synthetic self-assembled structures, are poorly understood. We have used a model system consisting of microtubules (MTs) and multivalent cations to examine how microscopic interactions can give rise to distinct bundle phases in biological polyelectrolytes. The structure of these supramolecular assemblies was elucidated on length scales from subnanometer to micrometer with synchrotron x-ray diffraction, transmission electron microscopy, and differential interference contrast microscopy. Tightly packed hexagonal bundles with controllable diameters were observed for large trivalent, tetravalent, and pentavalent counterions. Unexpectedly, in the presence of small divalent cations, we have discovered a living necklace bundle phase, comprised of 2D dynamic assemblies of MTs with linear, branched, and loop topologies. This new bundle phase is an experimental example of nematic membranes. The morphologically distinct MT assemblies give insight into general features of bundle formation and may be used as templates for miniaturized materials with applications in nanotechnology and biotechnology.
Bibliography:Abbreviations: MT, microtubule; MAP, MT-associated protein; SAXRD, small-angle x-ray diffraction; TEM, transmission electron microscopy; DIC, differential interference contrast; Cc, critical concentration.
To whom correspondence should be addressed. E-mail: safinya@mrl.ucsb.edu.
Author contributions: D.J.N. and C.R.S. designed research; D.J.N., M.A.O.-L., and U.R. performed research; D.J.N. and C.R.S. analyzed data; H.P.M. and L.W. contributed new reagents/analytic tools; and D.J.N. and C.R.S. wrote the paper.
This paper was submitted directly (Track II) to the PNAS office.
Edited by David Chandler, University of California, Berkeley, CA, and approved September 30, 2004
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.0406076101